Bacterial/archaeal/organellar polyadenylation

Abstract

Although the first poly(A) polymerase (PAP) was discovered in Escherichia coli in 1962, the study of polyadenylation in bacteria was largely ignored for the next 30 years. However, with the identification of the structural gene for E. coli PAP I in 1992, it became possible to analyze polyadenylation using both biochemical and genetic approaches. Subsequently, it has been shown that polyadenylation plays a multifunctional role in prokaryotic RNA metabolism. While the bulk of our current understanding of prokaryotic polyadenylation comes from studies on E. coli, recent experiments with Cyanobacteria, organelles and Archaea, although limited, have widened our view on the diversity, complexity, and universality of the polyadenylation process.For example, the identification of polynucleotide phosphorylase (PNPase), a reversible phosphorolytic enzyme that is highly conserved in bacteria, as an additional PAP in E. coli caught everyone by surprise. In fact, PNPase has now been shown to be the source of post-transcriptional RNA modifications in a wide range of cells of prokaryotic origin including those that lack a eubacterial PAP homologue. Accordingly, the past few years have witnessed increased interest in the mechanism and role of post-transcriptional modifications in all species of prokaryotic origin. However, the fact that many of the poly(A) tails are very short and unstable as well as the presence of polynucleotide tails has posed significant technical challenges to the scientific community trying to unravel the mystery of polyadenylation in prokaryotes. This review discusses the current state of knowledge regarding polyadenylation and its functions in bacteria, organelles and Archaea. Keywords poly(A) polymerase; polynucleotide phosphorylase; Hfq; RNA degradation Polyadenylation is a post-transcriptional event that involves the addition of untemplated adenosine residues to the 3' ends of RNA substrates. The first bacterial poly(A) polymerase (PAP) was identified almost 50 years ago in Escherichia coli [1,2]. A PAP was also identified in eukaryotic cells at about the same time [3,4]. However, polyadenylation in bacteria was virtually ignored for next 30 years, in part because eukaryotic poly(A) tails were relatively long, nearly uniform in length, and were found on almost all mRNAs. Furthermore, even though poly(A) tails were detected in E. coli and Bacillus subtilis [5][6][7][8][9], the overall low abundance of polyadenylated transcripts and the apparent lack of evidence for a physiological role led to the belief that polyadenylation was only important in higher organisms (See definition of polyadenylation in the glossary of Lewin, Genes I through Genes VIII).* To whom correspondence should be addressed. NIH Public Access Author ManuscriptWiley Interdiscip Rev RNA. Author manuscript; available in PMC 2011 September 27. Published in final edited form as:Wiley Interdiscip Rev RNA. 2010 September 27; 2(2): 256-276. doi:10.1002/wrna.51. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscri...

RNase E forms a complex with polynucleotide phosphorylase in cyanobacteria via a cyanobacterial-specific nonapeptide in the noncatalytic region

“…Polyadenylation at the 3 ′ -end is the prerequisite for normal metabolism of many RNA species in prokaryotes (Mohanty and Kushner 2011). In E. coli, RNA polyadenylation, which is able to stimulate substrate decay by the degradosome, is carried out primarily by the nondegradosomal enzyme poly (A) polymerase (Blum et al 1999;Mohanty and Kushner 1999;Khemici and Carpousis 2004).…”

Defects in RNA polyadenylation impair both lysogenization by and lytic development of Shiga toxin-converting bacteriophages

“…This process occurs in both eukaryotic and prokaryotic cells, while having different consequences in these two groups of biological entities (see Mohanty & Kushner, 2011 for a review). In bacteria, it is generally assumed that polyadenylated RNA molecules are more susceptible to degradation, thus addition of poly(A) tails destabilizes various transcripts.…”

“…In bacteria, it is generally assumed that polyadenylated RNA molecules are more susceptible to degradation, thus addition of poly(A) tails destabilizes various transcripts. However, there are also examples of RNA stabilization upon polyadenylation, which makes the control of RNA metabolism even more complicated (Mohanty & Kushner, 2011;Régnier & Hajnsdorf, 2013). Moreover, although it was initially believed that RNA polyadenylation in bacterial cells concerns mainly (if not exclusively) mRNA and small regulatory RNA (sRNA) species, recent reports indicate that this kind of modification of tRNA molecules may have an important impact on cell physiology (Mohanty et al, 2012;Mohanty & Kushner, 2013).…”

“…Moreover, although it was initially believed that RNA polyadenylation in bacterial cells concerns mainly (if not exclusively) mRNA and small regulatory RNA (sRNA) species, recent reports indicate that this kind of modification of tRNA molecules may have an important impact on cell physiology (Mohanty et al, 2012;Mohanty & Kushner, 2013). In E. coli, the major enzyme responsible for RNA polyadenylation is poly(A) polymerase I (PAP I), encoded by the pcnB gene (Cao & Sarkar, 1992;Mohanty & Kushner, 2011). Transcripts derived from over 90 % of ORFs undergo polyadenylation by this enzyme to some extent (Mohanty & Kushner, 2000.…”

“…Because the field studying the role of polyadenylation in the development of bacteriophages is clearly underexplored and in the light of mounting evidence for important regulatory functions of this RNA modification (Mohanty & Kushner, 2011;Régnier & Hajnsdorf, 2013), we aimed to investigate the effects of mutating the pcnB gene, coding for the major E. coli poly(A) polymerase, on lytic and lysogenic modes of development of Shiga toxin-converting bacteriophages.…”